Animal breeding systems and big game hunting: Models and application 5

BIOLOGICAL CONSERVATION 142 (2009) 909 929 available at www.sciencedirect.com journal homepage: www.elsevier.com/locate/biocon Animal breeding systems and big game hunting: Models and application 5 T.M. Caro a, *, C.R. Young b,c,1, A.E. Cauldwell d, D.D.E. Brown e a Department of Wildlife, Fish and Conservation Biology and Center for Population Biology, University of California, Davis, CA 95616, USA b Department of Ecology and Evolutionary Biology, University of California, 1156 High Street, Santa Cruz, CA 95064, USA c Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA d Kagera Kigoma Game Reserves Rehabilitation Project (EDF), P.O. Box 77, Kibondo, Tanzania e Animal Behavior Graduate Group, University of California, Davis, CA 95616, USA ARTICLE INFO ABSTRACT Article history: Received 31 March 2008 Received in revised form 11 December 2008 Accepted 14 December 2008 Keywords: Harem size Harvest models Infanticide Exploitation Large mammals Paternal care We apply an age- and stage-structured model incorporating varying harem sizes, paternal care and infanticide to examine the effect of hunting on sustainability of populations. Compared to standard carnivore and herbivore models, these models produce different outcomes for sustainable offtake when either adults, or adult males are harvested. Larger harem size increases sustainable offtake whereas paternal care and infanticide lowers it. Where males are monogamous, populations are vulnerable to male offtake, regardless of paternal care. Surprisingly, an incidental take of 10% of other age sex-classes has very little effect on these findings. Indiscriminate (subsistence) hunting of all age sex classes has a dramatic effect on certain populations. Applying these behavior sensitive models to tourist hunting in the Selous Game Reserve, Tanzania, we find that across the Reserve hunting quotas were generally set at sustainable rates except for leopard (Panthera pardus). In certain hunting blocks within the Reserve, however, quotas for eland (Taurotragus oryx), hartebeest (Alcelaphus buselaphus), lion (Panthera leo), reedbuck (Redunca arundinum), sable antelope (Hippotragus niger), warthog (Phacochoerus aethiopicus) and waterbuck (Kobus ellipsiprymnus) are set at unsustainably high rates. Moreover, particular blocks are consistently awarded high quotas. Behaviorally sensitive models refine predictions for population viability, specify data required to make predictions robust, and demonstrate the necessity of incorporating behavioral ecological knowledge in conservation and management. Ó 2008 Elsevier Ltd. All rights reserved. 1. Introduction Organized hunting of wild animals for sport can have considerable conservation benefits (Taylor and Dunstone, 1996; Lewis and Alpert, 1997; Hurt and Ravn, 2000; Reynolds et al., 2001; Lewis and Jackson, 2005; Lindsey et al., 2007). For example, in Eastern and Southern Africa it is widely recognized that areas set aside for hunting big game animals protect 5 Responsibilities: TMC devised and coordinated the project, helped collate life history parameters, breeding system data and densities, and wrote and revised the bulk of manuscript; CRY analyzed the models and wrote parts of methods and results pertaining to the models; AEC collected the Selous hunting data; DDEB collated life history parameters and densities. * Corresponding author: Tel.: +1 530 752 0596; fax: +1 530 752 4154. E-mail addresses: tmcaro@ucdavis.edu (T.M. Caro), cyoung@oeb.harvard.edu (C.R. Young), Andrew@eduaccess.co.za (A.E. Cauldwell), ddebrown@ucdavis.edu (D.D.E. Brown). 1 Present address: Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA. 0006-3207/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2008.12.018

910 BIOLOGICAL CONSERVATION 142 (2009) 909 929 habitats that might otherwise be turned over to agriculture (Pelkey et al., 2000), protect populations of large mammals (Caro et al., 1998a) and can benefit local people (Eltringham, 1984; Bond, 2001; Borgerhoff Mulder and Coppolilllo, 2005). Nonetheless, exploitation of the populations of particular species always has the potential to reduce population sizes to levels at which hunting is no longer economically profitable or even to cause population extinction in extreme cases (Adams, 2004). Unfortunately, it is difficult to estimate animal population sizes and to monitor them over time, and in most parts of the world hunting quotas are set through informed guesswork (Baldus and Cauldwell, 2004). Therefore it would be helpful from both an ecological and economic point of view to set hunting industries on a firmer scientific footing. This is particularly true in Africa where it is difficult to provide the scientific input needed for good management. The impact of hunting on animal populations depends on several factors that include age of individuals removed, sex and reproductive condition, and, of course, the number of individuals taken (Festa-Bianchet, 2003). In an effort to regulate hunting, most countries have laws that pertain to these variables that include restricting offtake to adults or to adult males, to certain times of the year, and setting strict limits on the number of animals that hunters may shoot. In some countries, hunting seasons are tailored to each species, as in the USA, whereas in others, one hunting season pertains to all species and must necessarily be a compromise in protecting the reproductive interests of different species. Recently, it has been recognized that the breeding system of the population being exploited can also affect the ability of the population to respond to hunting pressure (Milner et al., 2007; Price and Gittleman, 2007). For example, modeling shows that populations of monogamous species and species in which males commit infanticide are particularly susceptible to removal of males (Greene et al., 1998; Whitman et al., 2004). In practice, however, the rules surrounding hunting are difficult to enforce (Lindsey et al., 2007). While it is relatively easy to limit legal hunting to particular seasons, it is more difficult to ensure that hunting quotas are adhered to and that only certain age sex classes are taken. This is particularly evident when sexes are difficult to distinguish, or more unfortunately, when hunters are unscrupulous and take more than their allocation (Caro and Baldus, 2006). The purpose of this paper is to explore the way in which hunting practice has the potential to affect animal populations in East Africa when their breeding systems are taken into account. In order to highlight the effects of hunting policy on animal populations, we focus on tourist hunting practices in the largest game reserve in the world, the Selous Game Reserve in Tanzania, where hunting is an important economic activity (Baldus and Cauldwell, 2004; Cauldwell, 2004; Leader-Williams et al., 1996). Building on a previous modeling exercise (Young and Towbin, submitted for publication), we address how different degrees of hunting offtake affect the intrinsic rate of population increase in species where males help in rearing offspring, in species where males commit infanticide and in species where harem size varies. We have chosen these three criteria for the following reasons. (1) When game policy was being developed in Tanzania in the 1970s, scientists and laypeople believed that females were solely responsible for raising offspring; behavioral ecologists now know that male care is important in many species (Clutton-Brock, 1991). (2) At that time, infanticide by extra-group males was unknown. The first documentation of it was by Bertram (1975) for lions but it is now suspected for several other species (Breden and Hausfater, 1990). (3) If species exhibit paternal care, population growth rates are reduced, and this effect interacts with hunting policy (Young and Towbin, submitted for publication). (4) Harem size is known to affect sustainable harvest (Greene et al., 1998). 1.1. Background to tourist hunting in Tanzania Tanzania has set aside 180,000 km 2 for tourist hunting and offers a large number of species for sport hunting, principally mammals, but also upland birds (Tanzania Wildlife Conservation Act, 2002); it is the most popular big game hunting country in Africa (Lindsey et al., 2006, 2007). In practice, a hunting company takes out a lease on one or several hunting blocks which are segments of a Game Reserve, Game Controlled Area or Open Area, and the company is allocated a speciesspecific hunting quota for the season. A portion of this quota is then offered to clients who come to stay at hunting camps for 1, 2 or 3 week long periods. Clients sometimes fly between different hunting blocks leased by the same company in order to shoot species found only in certain parts of the country but quotas pertain to a hunting block. Hunting season commences on July 1st each year and ends on December 31st. In most parts of southern Tanzania where many of the hunting blocks are found, the effective hunting season finishes in November when the rains begin and roads become impassable (Baldus and Cauldwell, 2004). Tourist hunters are allowed to shoot a large number of game species (Table 1). In 15 species with marked sexual dimorphism, only males can be taken, but in most other species both sexes can be shot providing females are not believed to be pregnant, nursing or accompanied by dependent young (Tanzania Wildlife Conservation Act, 1974). Tanzanian residents are allowed to shoot a total of 22 species for meat. In six of these species, only males are legally hunted but for the other 16 species animals of any age sex class can be shot (Table 1). The paper is organized as follows. Having documented those species that are hunted in Tanzania, and in particular in Selous, we next describe the breeding systems of the 24 most commonly sought after species in Selous and, for the sake of generality, collapse them into two different carnivore breeding system types and eight herbivore types. We then examine sustainable offtake predicted by the 10 model formulations specifically tailored to these breeding systems. For each of these scenarios, we determine the effect of incidental hunting on sustainable offtake. At the end of the paper, we compare the output of these models to hunting quotas and actual hunting offtake of the 24 species in the Selous in order to determine whether current hunting practices are more or less sustainable than the predictions that arise from the models. This exercise also highlights which hunting blocks are being awarded overly generous hunting quotas. Finally, we suggest which species may require new hunting

BIOLOGICAL CONSERVATION 142 (2009) 909 929 911 Table 1 Game species of mammals listed in the fourth schedule of the Tanzania Wildlife Conservation Act, 1974 together with listed scientific names and hunting policy. Species hunted in Selous are shown in italics. Common name Scientific name Legally hunted by Tourists A Residents A Baboon olive Papio anubis MF Baboon yellow Papio cynocephalus MF Buffalo Syncerus caffer M All Bushbuck Tragelaphus scriptus M All Bushpig Potamochoerus porcus MF Caracal Felis caracal MF Cat civet Civetiictis civetta MF Cat genet Genetta genetta MF Cat serval Felis serval MF Cat wild Felis lybica MF Dikdik Rynchotragus kirkii MF All Duiker Abbots Cephalophus spadix MF All Duiker blue Cephalophus monticola MF All Duiker common Sylvicapra grimmia MF All Duiker red Cephalophus natalensis MF Eland Taurotragus oryx M M Elephant Loxodonta africana MF B Galago Galago senegalensis MF Fox bat-eared Otocyon megalotis MF Gazelle Grant s Gazella grantii M M Gazelle Thomson s Gazella thomsonii M M Gerenuk Litocraneous walleri M Giraffe C Giraffa camelopardalis Hare African Lepus capensis MF All Hare jumping Pedetes surdaster MF Hartebeest Coke s a Alcelaphus buselaphus cokei MF All Hartebeest Lichenstein s a Alcelaphus buselaphus lichensteinii MF All Hippopotamus Hippopotamus amphibius MF Hedgehog Erinaceus preuneri MF Hog giant forest Hylochoerus meinertzhageni MF Hyena spotted Crocuta crocuta MF Hyrax rock Heterohyrx procavia MF All Hyrax tree Dendrohyrax aboreous MF Impala Aepyceros melampus M M Jackal golden Canis aureus MF Jackal striped Canis adustus MF Jackal silver-backed Canis mesomelas MF Klipspringer Oreotragus oreotragus MF Kudu greater Strepsiceros strepsiceros M Kudu lesser Strepsiceros imberbis M Leopard Panthera pardus M Lion Panthera leo M Mongoose Viverridae MF Monkey colobus (b and w) C Colobus spp. MF Monkey blue Cercopithecus spp MF Monkey Sykes C Cercopithecus spp. MF Monkey vervet Cercopithecus aethiops MF Oribi Ourebia ourebi MF All Oryx Oryx gazella MF Otter Aonyx lutra MF Pigmy antelope (suni) Nesotragus moschatus MF All Porcupine Hystrix galeata MF Puku Adenota vardoni M Ratel Mellivora capensis MF Reedbuck bohor b Redunca redunca M M Reedbuck mountain Redunca fulvorufula M Reedbuck southern b Redunca arundinum M M Rhinoceros C Diceros bicornis Roan antelope Hippotragus equinnus M Sable antelope Hippotragus niger M Sharpe s grysbok Nototragus sharpei MF (continued on next page)

912 BIOLOGICAL CONSERVATION 142 (2009) 909 929 Table 1 Continued Common name Scientific name Legally hunted by Tourists A Residents A Sitatunga Tragelaphus spekei M Steinbuck Raphiceros campestris M All Topi Damaliscus korrigum jimela MF All Warthog Phacochoerus aethiopicus MF All Waterbuck common c Kobus ellipsiprymus M Waterbuck defessa c Kobus defessa M Wild dog# Lycaon pictus Wildebeest Nyasa d Connochaetes taurinus taurinus MF All Wildebeest white-bearded d Connochaetes taurinus albojubatus MF All Zebra Equus burchelli MF Zorilla Inctonyx striatus MF A M: adult males, F: adult females and All: all age sex classes. B Only elephants with tusks each over 20 kgs. C These species can no longer be legally hunted. a d Treated as the same species in analyses. restrictions as a result of incorporating behavioral ecological knowledge about their specific breeding system. 2. Methods 2.1. Study area The Selous Game Reserve is a World Heritage Site situated in southeastern Tanzania (Fig. 1), and covers approximately 45,000 km 2, about the size of Ireland. Much of it is drained by the Rufiji River formed after the Luwegu and Kilombero Rivers join; it also has three major tributaries, the Luhombero, Njenje and Mbarang andu, that join it within the Reserve. The southeast is drained by the Matandu River. The east receives approximately 750 mm or rain per year, the west 1300 mm. The northern sixth of the Reserve is open wooded grassland dominated by Terminalia spinosa and Hyphaene thebaica, and by Borassus aethiopium along the rivers. The southern 5/6th of the Reserve is deciduous miombo woodland with Brachystegia spiciformis, B. boehmii dominating, as well as Julbernardia globiflora, Pterocarpus angolensis, Dalbergia melanoxylon, Isoberlinia spp., Diplorhyncus condylocarpus and Combretum spp. This occurs as closed woodland and dense thickets in the centre and south, as open woodland in the west, and as scattered Fig. 1 Location of the Selous Game Reserve in Tanzania.

BIOLOGICAL CONSERVATION 142 (2009) 909 929 913 Fig. 2 Detail of Selous Game Reserve hunting blocks. National Parks (Mikumi and Udzungwa) are shown in light grey; Kilombero Game Controlled Area, and Kilwa and Liwale Open Areas in medium grey. tree grassland in the east (see Creel and Creel (2002) and Stephenson (1990) for details). For tourist hunting purposes, the Game Reserve is divided into 47 hunting blocks and there are adjacent Game Controlled Areas and Open Areas where hunting is allowed (Fig. 2). The Selous alone generates 35% of the tourist hunting income for the Government of Tanzania (Baldus and Cauldwell, 2004; Kibonde, 2006). 2.2. Species classifications We used the Tanzania Wildlife Act of 1974 and AEC s data on Selous quotas and offtake 1988 1997 to determine the species hunted in Selous and the hunting policies for both tourist and resident hunters (Table 1). Then, using authoritative guides for African mammals, Estes (1991), Kingdon (1997), Nowak (1999) and Stuart and Stuart (2001), legally hunted species were first classified according to whether adult males provide parental care either through regular offspring defense or through food provisioning. Next, species were classified as to whether males are known to commit infanticide, a behavior that may occur when new males usurp harem holders or when males encounter a harem where there are no biological fathers to defend the group; male territorial defense of cubs therefore came under this heading. Finally, species were classified according to harem size (Table 2). Harem sizes determine whether reproduction is male or female-limited, and can substantially alter predictions of population responses to hunting pressures (Greene et al., 1998; Young and Towbin, submitted for publication). 2.3. Standard and tailored models We applied an age sex structured density independent model to determine maximum sustainable harvest for a variety of parameterizations and hunting policies (details in Young and Towbin, submitted for publication). We chose to use a density independent model because we assumed that, in contrast to populations in national parks, hunted populations are not likely to be at carrying capacity or limited by resources due to sustained hunting pressure from both legal tourist hunting and illegal hunting (Holmern et al., 2007). The model allows a variable number of stage- and sex-specific age classes (j m : number of juvenile male cohorts, j f : juvenile female cohorts, a m : adult male cohorts, a f : adult female cohorts) as well as stage- and sex-specific survival rates for male and female birth-class individuals (s M and s F, respectively), male and female juveniles (r M and r F ), and male and female adults (q M and q F ) (see Fig. 3). Inaccuracies in longevity estimates have little effect on reproductive output because of low survival probabilities in old animals. Various aspects of species breeding systems are also included in subsequent iterations of the model, including fecundity (m), harem size (h), both paternal (p M ) and maternal (p F ) care, and infanticide (p) with time steps measured in inter-birth intervals with survivorship parameters corresponding to the species particular inter-birth interval (Young and Towbin, submitted for publication). Hunting policies defined by legally hunted stage sex classes include: adult males, or both male and female adults. Indiscriminate and illegal subsistence hunting of all age sex classes also occurs. A particular hunting policy also includes an offtake level, defined as the proportion of the total population that is harvested, p h. In our model analyses, we use the conventional but arbitrary maximum sustainable yield for a species as the largest offtake level for which population growth rates remain positive, k > 1. In addition to the legally hunted classes, we allow a proportion of encounters, p I, to result in deaths of individuals mistakenly identified as legal. We assume that these additional kills are incidental take and do not count towards the legal offtake level. When included in the model, we assumed that p I = 0.10. We chose this figure as a rough balance between hunters taking more than 10% of females or juveniles and not declaring them on the one hand, and hunters reporting some of this incidental take as legal offtake, on the other, bearing in mind that data on illegal hunting bags are unavailable at present. For leopards (Panthera pardus), we assume an incidental take of p I = 0.30 because genetic studies have determined that about 30% of the leopards killed in Tanzania are female (Spong et al., 2000). We consider archetypal large carnivores and large herbivores defined by what is necessarily an amalgamation of different survival rates and fecundities of various species. We first consider a standard model for each of these archetypes in which species are monogamous, provide no paternal care, and do not commit infanticide. We do this for illustrative purposes, namely to demonstrate the shortcomings of using population models that do not incorporate information on animal breeding systems. We then tailor these two standard or generic models to correspond to common breeding systems found among hunted species in the Selous (Table 3). Survivorship, numbers of stage age classes, and fecundities are the same for the standard and tailored models. The carnivore survival rates are defined as: s M = 0.7, s F = 0.7, r M = 0.8, r F = 0.8, r M = 0.8, and r F = 0.9. The number

914 BIOLOGICAL CONSERVATION 142 (2009) 909 929 Table 2 Aspects of breeding systems of game species (mammals) hunted by tourists in Tanzania. Offspring accompany parent during hunting season? Male of care offspring? Infanticide by males? Group size Baboon a Yes No Yes >5 Buffalo Yes No No >5 Bushbuck Yes No No 2 5 Bushpig Yes No No 2 5 Caracal Yes/No No Yes? 1 Cat b Yes/No No No? 1 Dikdik Yes Yes No 2 5 Duiker c Yes Yes? No 2 5 Eland d Yes No No >5 Elephant Yes No No >5 Galago Yes No? No 1 Fox bat-eared Yes/No Yes No 2 5 Gazelle Grant s d Yes No No >5 Gazelle Thomson s d Yes No No >5 Gerenuk d Yes No No 2 5 Hare African No No No 1 Hare jumping No No No 1 Hartebeest Yes No No >5 Hippopotamus Yes/No No Yes >5 Hedgehog No No No 1 Hog giant forest Yes No No 1 Hyena spotted Yes/No No No >5 Hyrax rock Yes/No No No >5 Hyrax tree No No No 1 Impala d Yes No No >5 Jackal e Yes/No Yes No 2 5 Klipspringer Yes/No Yes No 2 5 Kudu greater d Yes No No 2 5 Kudu lesser d Yes No No 2 5 Leopard d Yes/No No Yes? 1 Lion d Yes/No No Yes >5 Mongoose Yes/No Yes f /No g No 1 g />5 f Monkey blue Yes No Yes? >5 Monkey vervet Yes No No >5 Oribi Yes Yes No 2 5 Oryx Yes No No >5 Otter Yes/No Yes? No 1? Pigmy antelope Yes Yes No 2 5 Porcupine Yes No? No 2 5 Puku d Yes No No >5 Ratel Yes/No No? No 2 5 Reedbuck h Yes No No 2 5 Roan d Yes No No >5 Sable d Yes No No >5 Sharpe s grysbok Yes Yes? No 2 5? Sitatunga Yes No No 2 5? Steinbuck Yes Yes No 2 5 Topi Yes No No >5 Warthog Yes No No >5 Waterbuck d Yes No No >5 Wildebeest Yes No No >5 Zebra Yes No Yes >5 Zorilla Yes/No No? No 2 5? a Olive and yellow baboon combined. b Civet, genet, serval and wildcat combined. c Abbots, blue, common and red combined. d Species in which only adult males can be legally shot. e Golden, black-backed and side-striped combined. f Dwarf and banded mongoose;. g Slender, grey, white-tailed and marsh mongoose species. h Bohor, mountain and southern combined.

BIOLOGICAL CONSERVATION 142 (2009) 909 929 915 Fig. 3 (A) The stage age structured model of Young and Towbin (submitted for publication). The model tracks the demography of the sexes separately. Age classes (boxes corresponding to reproductive cohorts) are classified by the birth, juvenile and adult stages. The model tracks the numbers of individuals belonging to each age class. The stages have stagespecific survival rates (s, r, and q) that determine the fraction of individuals that move to the adjacent age class in the next generation in the absence of hunting. Hunting policy defines which stage sex classes are legal to hunt (i.e., adult males, adults of both sexes, or subsistence hunting that allows juveniles and adults of both sexes to be hunted) and the hunting pressure applied to the population (i.e., quota). (B) The temporal order of calculations is for a single generation of the model. Mortality is first calculated based on the natural survival rates (s, r, and q), hunting mortality, and mortality of individuals in the birth class due to infanticide or parental care. After mortality, the remaining adults are collected into breeding groups (e.g., harems or monogamous pairs), and are allowed to reproduce (i.e., add individuals to the next time step s birth class). Finally individuals are shifted one age class to the right, and the population census is taken. Table 3 Selous species categorizations for tailored models; species known or suspected of being infanticidal are in italics. Paternal Care Yes No Approximate harem size 1 2 5 1 5 10 Klipspringer Suni Zebra Leopard Lion Hippopotamus Warthog Oribi Bushpig Ratel Waterbuck Hartebeest Duiker Porcupine Bushbuck Wildebeest Jackal Steinbuck Greater Kudu Sable Reedbuck Impala Roan Eland Buffalo Puku Elephant Parental care refers to males maintaining a territory around females, maintaining vigilance for mates and their offspring, or being involved in antipredator defense of their offspring. of cohorts in each carnivore stage sex class are: j m =3,j f =2, a m =8, a f = 13; juvenile males take longer to reach sexual maturity than females so we ascribed them an additional juvenile cohort. We assumed an average fecundity of 2.5 offspring per reproductive female per inter-birth interval. We always assumed that carnivores are monogamous (i.e., harem size, h = 1). The herbivore survival rates are defined as: s M = 0.8, s F = 0.8, r M = 0.85, r F = 0.85, q M = 0.875, and q F = 0.925. The number of cohorts in each herbivore stage sex class are: j m =2, j f =2, a m = 10, a f = 12. We assumed an average fecundity of one offspring per reproductive female per inter-birth interval. Harem size was variable under the herbivore scenario (i.e., h = 1, 2, 5, or 10). Note, life history variables for the carnivore and herbivore were a conglomeration of parameters of many species ranging, for instance, from leopard (Panthera pardus) to zorilla (Inctonyx striatus), and eland (Taurotragus oryx) to oribi (Ourebia ourebi) and are therefore modal values of well-worked species, poorly known species and best guesses. In short, we made a conscious decision to sacrifice accuracy in life tables of a handful of wellworked species for general conclusions about most of the important larger mammals hunted in Tanzania. Infanticide, maternal care, and paternal care, when included, were parameterized as: p = 1.0 (i.e., the extreme case

916 BIOLOGICAL CONSERVATION 142 (2009) 909 929 where death of a reproductive male always leads to the death of that male s offspring due to infanticide), p M = 1.0 (i.e., the severe case where male mortality always leads to the death of a male s offspring due to lack of paternal care) and p F = 1.0 (i.e., female mortality always leads to the death of a female s offspring due to lack of maternal care). All of the tailored models include maternal care because this is ubiquitous in mammals. Therefore, the realized birth-class survival (i.e., accounting for infant mortality due to natural maternal mortality), calculated using Eqs. (44) (49) in Young and Towbin (submitted for publication), is 0.63 for carnivores and 0.74 for herbivores. If paternal care is included in the model, natural adult mortality produces a realized birth-class survival of 0.50 for carnivores and 0.65 for herbivores. The realized birthclass survivorship under maternal care (s F = 0.63) as well as juvenile (q F = 0.85) and adult survival rates (q F = 0.925) are similar to observed rates for buffalo (Synerus caffer) (s F = 0.67, r F = 0.86, q F = 0.93) and wildebeest (Connochaetes taurinus) (s F = 0.75, r F = 0.89, q F = 0.79) in the Serengeti (Grange et al., 2004). The reduction in realized birth-class survival for species exhibiting paternal care is similarly observed in zebra (Equus burchelli) on the Serengeti, although in our parameterization, realized birth-class survival is higher than estimates for Serengeti zebra (95% confidence interval of s = 0.30 0.48; Grange et al., 2004). For African mammals, there are actually rather few commonly hunted species for which other life history variables are known to which we can verify our model parameter values. 2.4. Population estimation and actual hunting intensities In order to compare model results to actual hunting offtake occurring in Selous, for some species we collated density estimates from aerial census data that have been carried out by Tanzania Wildlife monitoring teams over the Selous; these counts are not age or sex-specific. These estimates were the averages of the October 1986, September 1989, June 1991, September 1994, October 1998 and October 2002 censuses (Caro, 2005; Stoner et al., 2007) resulting in one population estimate for each species in the Selous. We used these estimates for eland, greater kudu Tragelaphus strepsiceros, hartebeest (Alcelaphus buselaphus), hippopotamus (Hippopotamus amphibius), puku (Kobus vardonii), sable antelope (Hippotragus niger), waterbuck (Kobus ellipsiprymnus), wildebeest and zebra. These are the best available population data that we have for these species at present because permission is not granted to conduct ground surveys in the hunted part of the Selous Game Reserve. For other species that are difficult to count from the air (Caro et al., 2000), we used density estimates from a foot survey conducted in three hunting blocks in a miombo habitat similar to the Selous, in the Rukwa Game Reserve of western Tanzania (Waltert et al., 2008). These species were bushbuck (Tragelaphus scriptus), bushpig (Potamochoerus porcus), common duiker (Sylivcapra grimmia), impala (Aepyceros melampus), reedbuck (Redunca arundinum), and warthog (Phacochoerus aethiopicus). For elephant (Loxodonta africana), we used the up-to-date figure from Baldus (2006). For klipspringer (Oreotragus oreotragus), oribi, steenbok (Raphicerus campestris) and suni (pigmy antelope) (Neotragus batesi), we arbitrarily divided the Rukwa small antelope density by four. In addition, for buffalo, we used the Rukwa density of 1.6/km 2 rather than the average aerial census density of 2.0/km 2 because, one author, AEC, who has extensive field experience of buffalo in Selous, felt the latter figure was too high. For lions (Panthera leo), we used data from in depth studies in Selous (Creel and Creel, 1996); for leopards, we used Estes (1991). We then generated a total estimated population size for each block by multiplying density by block area taken from Cauldwell (2004). All these estimates are necessarily crude but they are the best available at present. Next, we compared sustainable offtake that we operationally defined as the percentage of the population, for which k > 1, as predicted by the tailored models with (a) the percentage of the block population allocated for hunting and (b) the percent of the block population that was actually taken by hunters as based on Tanzania Wildlife Division inventory records averaged across years 1988 1997. This enabled us to determine whether permissible offtake and actual offtake exceeded or fell below calculated sustainable offtake. The model did not include interactions between population size and hunting success because we assumed hunters would continue to fill their quota based on their prior agreement with the hunting company rather than according to population abundance. 3. Results Of the 53 mammal game species or species constellations (e.g., mongooses) hunted by tourists in Tanzania, 35 give birth to offspring that accompany them during hunting season, four produce offspring that are not with them, leaving 14 species where information is equivocal as to whether offspring accompany their parents during this period (Table 2). Therefore there is a potential for hunters to shoot females with dependent young in a minimum of 66% of the species that they are allowed to shoot if they do not check whether females are lactating or have young close by. Males help care for offspring in 11 out of the 53 species, and it is notable that males may be legally shot in all of these 11 species! Infanticide by males is relatively uncommon. Infanticide occurs or is thought to occur in 7 out of 53 species. Males are exclusively targeted in only two of these species, lion and leopard. Of the 53 game species, 32 are solitary or live in large groups where removal of a single individual is unlikely to influence subsequent survival or reproduction of conspecifics, whereas perhaps 19 species live in small permanent groups of less than five animals where Allee effects (Allee, 1931) might become important as a result of the removal of an individual. Our model does not include Allee effects, and the results of our model should be interpreted with caution for species or populations in which Allee effects might be important. Focusing on species hunted in Selous, and separating species by whether males care for offspring, commit infanticide, or the species lives in small groups, the following pattern emerged (Table 3). Most Selous game species show no paternal care; the majority of species live in harems of 5 10 individuals, and few show infanticide. We now discuss the response to hunting of 24 of these species, omitting jackal species, ratel (Mellivora capensis) and porcupine (Hystrix galeata) which feature little in hunters bags.

BIOLOGICAL CONSERVATION 142 (2009) 909 929 917 Fig. 4 Standard carnivore and herbivore models. (A) Standard carnivore model: Effect of hunting quota (p h ) on population growth rates (k) under the three hunting policies (marked). (B) Standard herbivore model: Effect of hunting quota on population growth rates under the three hunting policies. (C) and (D) Standard carnivore and herbivore models respectively: Both panels show, for three different hunting policies (marked), the effect of increasing the hunting quota (p h )onthe proportion of the subpopulation that will be removed. Table 4 Model predictions of stable stage sex structure and female to male ratio under the carnivore and herbivore guild models (harem size = 1, no parental care, no infanticide, no incidental take). Guild Hunting policy MSY a Subpop. HI b Relative frequencies of stage sex classes c Female to male ratio % females in harems A m A f J m J f Adult Juv. Carnivore d No hunting 0.15 0.36 0.28 0.21 2.4 0.8 42 Male 0.018 0.121 0.12 0.44 0.25 0.19 3.8 0.7 27 Adult 0.063 0.121 0.15 0.30 0.32 0.23 2.0 0.7 49 Subsistence 0.062 0.062 0.14 0.34 0.29 0.22 2.4 0.8 42 Herbivore e No hunting 0.27 0.37 0.18 0.18 1.4 1.0 73 Male 0.023 0.094 0.22 0.47 0.16 0.16 2.2 1.0 46 Adult 0.062 0.094 0.26 0.35 0.20 0.20 1.3 1.0 76 Subsistence 0.063 0.063 0.26 0.36 0.19 0.19 1.4 1.0 74 a Maximum sustainable yield, as a proportion of the total population, under the specified hunting policy. b Subpopulation hunting intensity: proportion of the subpopulation harvested. c A m = adult male class, A f = adult female class, J m = juvenile male class, and J f = juvenile female class. d Juvenile female cohorts = 2, juvenile male cohorts = 3, adult female cohorts = 13, adult male cohorts = 8, and fecundity = 2.5. e Juvenile female cohorts = 2, juvenile male cohorts = 2, adult female cohorts = 12, adult male cohorts = 10, and fecundity = 1.0.

918 BIOLOGICAL CONSERVATION 142 (2009) 909 929 3.1. The standard models Young and Towbin (submitted for publication) develop a basic model that explores the response of population growth rates to hunting under three different hunting policies (Fig. 3). Here, we reexamine this basic model by parameterizing an archetypal large carnivore and large herbivore to address variation in life history parameters between these mammalian guilds. In the standard models, we assume no parental care, no infanticide and a harem size of one. In our model analyses, for simplicity we define the maximum sustainable yield as the largest quota for which population growth rates remain positive, k > 1. In practice, of course, it would be unwise to set quotas at or even close to this level. However, this boundary is a useful tool to compare the sustainability of hunting policies under different models. Our two standard models showed that hunters could remove 1.8% of the carnivore population if they shot only males, 6.3% if they shot both adult males and females, and 6.2% if they shot any age sex class before the population started to decline (Fig. 4A). For herbivores, they could remove 2.3% of the population if they killed only males, 6.2% if they shot both adult males and females, and 6.3% if they shot any age sex class (Fig. 4B). Adult and subsistence hunting policies under both the carnivore and herbivore models allow larger sustainable quotas than male hunting policies because male hunting alone shifts the age sex structure of the population. This is shown clearly in Table 4 where it can be seen that, even under no hunting, the population stage sex structure is skewed towards females (when male survival is lower than that of females and quite a large proportion of females are non-reproductive, see percent of females in harems column). In other words, the population is always reproductively male-limited when males have lower survival and the species is monogamous. With knowledge of the stationary age sex classes in the population for these hunting intensities, these maximum sustainable quotas correspond to 12.0% of the carnivore male subpopulation, 12.0% of the carnivore adult subpopulation, or 6.2% of the whole carnivore population as before (Fig. 4C). For herbivores, the above levels of offtake constitute 9.4% of the male subpopulation, 9.4% of the adult subpopulation, or 6.3% of the whole population (Fig. 4D). 3.2. The tailored models For our tailored models, we again divided our scenarios into two major categories, carnivores and herbivores. Next, we divided carnivores into two scenarios, lion and leopard, and, in the interests of conciseness, collapsed the 22 herbivore species into eight scenarios, Impala, Kudu, Steinbok, Hippo, Hartebeest, Zebra, Oribi and Warthog to incorporate differences in breeding system parameters (Table 5) clearly recognizing that this categorization ignores details of species-specific differences. The first five scenarios correspond to species in which only adult males are hunted, Table 5 Model predictions of stable stage sex structure and female to male ratio under the ten carnivore and herbivore models. Model h a Pat. care b Inf. c Hunting policy MSY d IT e (%) Relative frequencies of stage sex classes f Female to male ratio A m A f J m J f Adults Juv. Lion 5 N Y No hunting 0.13 0.30 0.32 0.25 2.3 0.8 Males 0.051 9.9 0.03 0.54 0.25 0.18 17.0 0.7 Leopard 2.5 N Y No hunting 0.13 0.30 0.32 0.25 2.3 0.8 Males 0.038 6.8 0.06 0.48 0.27 0.20 7.9 0.7 Impala 10 N N No hunting 0.26 0.35 0.19 0.19 1.3 1.0 males 0.068 5.9 0.04 0.49 0.24 0.24 12.6 1.0 Kudu 5 N N No hunting 0.26 0.35 0.19 0.19 1.3 1.0 Males 0.060 6.3 0.06 0.52 0.21 0.21 8.2 1.0 Steinbok 1 N N No hunting 0.28 0.40 0.16 0.16 1.4 1.0 Males 0.010 8.0 0.26 0.44 0.15 0.15 1.7 1.0 Hippo 10 N Y No hunting 0.27 0.36 0.18 0.18 1.4 1.0 Adults 0.051 5.9 0.27 0.36 0.19 0.19 1.3 1.0 Hartebeest 10 N N No hunting 0.26 0.35 0.19 0.19 1.3 1.0 Adults 0.071 5.9 0.26 0.34 0.20 0.20 1.3 1.0 Zebra 5 Y Y No hunting 0.27 0.36 0.18 0.18 1.4 1.0 Adults 0.051 5.9 0.27 0.36 0.19 0.19 1.3 1.0 Oribi 2 Y N No hunting 0.27 0.36 0.18 0.18 1.4 1.0 Adults 0.051 5.9 0.27 0.36 0.19 0.19 1.3 1.0 Warthog 1 Y N No hunting 0.28 0.40 0.16 0.16 1.4 1.0 Adults 0.021 6.7 0.28 0.40 0.16 0.16 1.4 1.0 a Harem size. b Paternal care: Y = included in the model, N = not included. Note: all models include maternal care. c Infanticide: Y = included in the model and N = not included. d Maximum sustainable yield, as a proportion of the total population, under the specified hunting policy. e Percent reduction in maximum sustainable yield assuming 10% of kills are incidental take (except for leopard, where 30% of kills are incidental). Incidental classes for each species are described in the text. f A m = adult male class, A f = adult female class, J m = juvenile male class, and J f = juvenile female class.

BIOLOGICAL CONSERVATION 142 (2009) 909 929 919 Fig. 5 Tailored models. Solid lines assume that incidental take, p I = 0. Dashed lines assume that incidental take, p I = 0.1; for leopards, p I = 0.3. Subsistences 1 and 2 are offtake of juveniles and adults of both sexes of warthog and buffalo, respectively. whereas the last five scenarios correspond to species in which adult males and females are hunted. 3.3. Carnivores Hunters are only allowed to shoot male lions. Coalitions of usually 2 3 male lions hold a pride of 5 10 females but show no paternal care as defined by regular care of offspring. When a coalition of males replaces another, the incoming coalition kills offspring fathered by the previous coalition. Since smaller coalitions are more likely to lose fights to larger coalitions, removal of a territorial male increases the probability of infanticide (Packer et al., 1988). We set harem size as five in the lion scenario. Hunting offtake can reach 5.1% of the population before the population growth rate declines to k <1(Fig. 5A). Therefore, the maximum sustainable quota under this scenario is 5.1%. If we add an incidental take of juvenile males because they are difficult to distinguish from adult males in the field, sustainable offtake is reduced to 4.6% (a 9.9% reduction). We do not consider an incidental take of females because the sexes are dimorphic and easily distinguishable, nor do we consider adult males <5 6 years old taking as incidental because males of this age are still allowed to be shot legally in Tanzania (Whitman et al., 2007). Tourist hunters are only legally allowed to shoot male leopards. Male leopards defend territories that overlap those of two to three female territories but they show no paternal care. Incoming males commit infanticide if they take over the territory of the current male. We set harem size as 2.5 in our leopard scenario. The maximum sustainable quota under this scenario is only 3.8% of the population (Fig. 5B). However, approximately 30% of the leopards killed in Tanzania are female (Spong et al., 2000). If we add a 30% incidental take of adult females, sustainable offtake is reduced to 3.6%. 3.4. Herbivores where adult males are shot Turning now to herbivores, tourist hunters are allowed to shoot males in strongly sexually dimorphic species, but adults of both sexes in many other species. The majority of herbivore species show no paternal care and no infanticide. We therefore separated herbivores into eight groups. Among buffalo, eland, impala, puku, and sable antelope, only males may be hunted. In these species, termed here the impala scenario, there is no paternal care, no infanticide, and these species are highly polygynous. We set harem size at 10 recognizing that this is an underestimate in some populations. Offtake here should not exceed 6.8% of the population if population is to remain viable (Fig. 5C). Adding an incidental take of 10% of juvenile males lowers the sustainable offtake to 6.4%. Among greater kudu, waterbuck, bushbuck, roan antelope Hippotragus equinus and reedbuck ( kudu scenario ), where hunters are similarly allowed to hunt only males, harem size is smaller, so we assumed a harem size of five. Again, there is no paternal care or infanticide. The maximum sustainable

920 BIOLOGICAL CONSERVATION 142 (2009) 909 929 quota for the kudu scenario is 6.0% (Fig. 5D). Allowing incidental take of juvenile males results in a sustainable hunting offtake of 5.6%. Adult males are legally hunted in steinbok. Steinbok are monogamous, so we assumed a harem size of one. There is no paternal care or infanticide. The maximum sustainable quota for this species is only 1.0% (Fig. 5E); incidental take of juvenile males results in a 0.9% sustainable offtake. This differs from the standard model because of maternal care. In all cases except steinbok, a male hunting policy alters the stationary age/sex structure of the population (Table 5). The steinbok stationary age/sex structure does not change much, because the species is monogamous and cannot tolerate high male hunting pressures. The rest of the herbivore models (below) assume adult hunting of both sexes which alters the stationary age/sex structure very little. 3.5. Herbivores where adult males and females are shot It is extremely difficult to tell male and female hippopotami apart because their testes are internal and they spend much time in water. In the hippopotamus scenario there is no paternal care but there is infanticide. Harem size is large, h = 10 (or more). The maximum sustainable quota for this species is 5.1% (Fig. 5F), which is reduced to 4.8% if incidental take of juvenile males and females is included. In hartebeest, wildebeest and elephant ( hartebeest scenario ), there is no paternal care, no infanticide, and harem size is large; we set it at 10. In this hartebeest scenario, k < 1 when offtake reaches 5.0% (Fig. 5G) and stays at 5.0% when incidental take is set at 10% juvenile males and females. In both zebra and bushpig ( zebra scenario ), infanticide has been reported anecdotally. In these species there is paternal care in the form of offspring defense, and harems are of medium size. We categorized these as five. In this zebra scenario, k > 1 when offtake reaches 5.0% (Fig. 5H) and stays at 5.0% when incidental take is set at 10% juvenile males and females. In the many duiker species, males show paternal care through antipredator vigilance, but there is no infanticide and these species are monogamous or bigamous. Thus for this oribi scenario, which includes species such as oribi, common duiker and suni, harem size is two. The proportion of the population that can be removed before the population declines is 5.1% (Fig. 5I), which is reduced to 4.8% when including incidental take of juvenile males and females. Warthog and klipspringer show paternal care, principally through antipredator defense, but there is no infanticide and harem size is one. The maximum sustainable quota for the warthog scenario is 2.1% (Fig. 5J). Adding a 10% offtake of juvenile males and females reduces the maximum sustainable quota to 2.0%. Model predictions for these 10 scenarios are summarized in Table 5. Note that while the exact date that a female with attendant offspring is shot will affect offspring survival probability, we did not attempt to model this. 3.6. Subsistence hunting We were also interested in modeling offtake based on subsistence hunting of warthog (paternal care, no infanticide, harem size = 1) because several studies have indicated that they are a favored food in the diet of poachers and that they are under threat across Tanzania (Stoner et al., 2007; Caro, 2008). Legal hunting offtake aside, warthog populations could withstand an offtake of only 2.3% if all age sex classes were taken (Fig. 5K). Similarly, poachers frequently target buffalo (no paternal care, no infanticide, harem size = 10). Independent of legal hunting, this species can sustain subsistence hunting offtake of up to 8.2% (Fig. 5L). 3.7. Tourist hunting quotas and offtake in Selous We now compare the predictions of these specific tailored models to hunting quotas and actual tourist hunting offtake across the whole Selous Game Reserve and then across individual hunting blocks for each of 22 species separately (roan antelope do not occur in Selous, and puku only occur in a very small area along Kilombero River to the extreme west and are not a significant game species in Selous). Perhaps optimistically we assumed that hunting is done professionally and therefore disregarded incidental take. Appendix A shows that across the whole Selous 20 species were allocated quotas less than calculated sustainable offtake and only one exceeded it. This was leopard. When the 43 hunting blocks were examined separately, however, it was apparent that certain species were allocated quotas that consistently surpassed calculated sustainable offtake based on tailored models and estimated population sizes in blocks. These were eland, hartebeest, leopard, lion, reedbuck, sable antelope, warthog, waterbuck and possibly steinbok. Some of these quotas were far larger than calculated sustainable offtake, notably leopard and lion, two of the species for which the greatest number of hunting blocks exceed calculated sustainable offtake. Despite these generous quotas, there were very few instances indeed where actual offtake was higher than calculated sustainable offtake and seven out of eight of these were in one hunting block, KY1/Gonabis. Indeed, for a number of species such as oribi, steinbok and suni (pigmy antelope), no kills were reported. Turning to the hunting blocks in Appendix A, there was great variability in the number of species for which quotas went above calculated sustainable offtake. In 22 out of 43 blocks, quotas of only one or none of the 21 species exceeded calculated sustainable offtake, whereas in two out of 43 blocks, 50% or more of species hunting quotas were over calculated sustainable offtake (elephant are not included on quotas as offtake is controlled by setting minimum trophy sizes). These blocks were M1 and U1, and quotas for the remaining 19 blocks were often consistently high across species. For instance, approximately one third of species quotas appeared high in blocks K3, K4, KY1/Gonabis, L1, LU5, M2, R3, and U2. These data on hunting blocks are more robust than data broken down by species because they rely less heavily on accurate densities for a given species. 4. Discussion Our goal in this paper was to parameterize the exploitation models of Young and Towbin (submitted for publication) to

BIOLOGICAL CONSERVATION 142 (2009) 909 929 921 make them applicable to large mammals hunted in the important game reserve of East Africa, the Selous. Since we are now assessing contemporary hunting practice that may be of interest to managers, and the Wildlife Division of Tanzania in particular, it is important to outline the shortcomings of these analyses at the outset. These analyses are timely given the attempts to certify the tourist hunting industry in Tanzania (Nshala, 1999). First, there are a number of difficulties with the parameterizations of the models. Notably, we approximated parameters for group sizes, fecundity, and sex ratio based on values taken from the literature that came from studies in many parts of Africa, frequently national parks or protected areas. Harem sizes and sex ratios may not always represent those in hunted areas in general or in the Selous specifically; moreover there is likely to be intrapopulation variation within the Selous itself. Furthermore, we had to estimate survival rates for both sexes, and this was very difficult as so few studies have examined survivorship in the wild. Our estimates are principally based on a handful of prominent studies from one or two species that we hope approximate other similar-sized species in the herbivore or carnivore guild. We did not attempt sensitivity analyses as these are beyond the scope of this paper, and they would be difficult to verify because so little is known about inter-population variability in life history parameters of most exploited species. Nonetheless, our parameters are satisfyingly similar to single species studies elsewhere with good data (e.g., Grange et al., 2004). We also made a number of assumptions about species densities. First, densities for large animals were derived from an average of aerial censuses conducted over a 15- year time span. Aerial censuses provide reasonably good estimates of larger mammals (Caro et al., 2000). For the smaller or more secretive herbivores, and also buffalo, we used a foot census from a different miombo area but nevertheless where big game hunting has occurred for many years, the Rukwa Game Reserve. For lion we used estimates from the northern Selous but from an unhunted area which will make predictions about this species rather generous. Finally, we took leopard density from the literature. While density estimates derive from diverse sources, there is no a priori evidence to suggest aerial or ground, Selous or non-selous sources show systematic bias for those species involved. In sum, there is no question that some of these density estimates are necessarily coarse and may even be optimistically large which would make our estimates of sustainable offtake generous. We used these densities to calculate population sizes in each hunting block, and this introduces further inaccuracies because blocks vary in types of habitat they support, some containing more open floodplains, others more rivers and so on. There are known soil and vegetation differences in the Selous Game Reserve but their relationship to animal densities is poorly understood. Applying a uniform density to each hunting block is therefore very coarse indeed. Nonetheless, in the absence of systematic surveys in each block, it is unfortunately the best approximation that we have. We wanted to focus on blocks because this is the level at which decisions are made by the Wildlife Division. Hunting offtake presents an additional problem. While hunting quotas are correct, offtake may not be entirely accurate due to documented reporting difficulties (Baldus and Cauldwell, 2004) with the magnitude of bias for different species unknown. Finally, although there is no resident hunting in Selous, which removes an unknown source of offtake, illegal hunting from nearby villages is common (Gillingham and Lee, 1999) and this may affect our conclusions. For example, if market forces change and demand for bush meat increases, then illegal hunting may reduce population sizes of certain species and thereby change sustainable tourist hunting offtake. Our assumptions are therefore three-tiered. There are concerns about the assumptions that went into the standard and tailored models, about estimating densities, and about accuracy of data on hunting practices. All of these will affect recommendations about hunting policy (Regan et al., 2005). Our exercise is an initial attempt to assess sustainability of hunting in a very important hunting area in Africa, an attempt that can and should be followed up if better data on offtake and population sizes become available. 4.1. Standard and tailored models The point at which a given level of offtake drives populations into decline is sometimes, but not always, strikingly different between standard and tailored models. The standard model assumes a harem size of 1 (h = 1) but higher harem sizes generally increase sustainable offtake. The other breeding details (paternal care and infanticide) reduce sustainable offtake. If then, a tailored model with say h = 5, maternal care only, and infanticide is compared with the standard model, the effects often, but not always, cancel each other out. The magnitude of these antagonistic effects will depend on the particular survival rates of the species, principally the difference in survival rates between males and females. In general, both standard and tailored models allowed for generous offtake levels between 2% and 7%; it is customary to set quotas much more cautiously at 2% of an estimated population size (Baldus and Cauldwell, 2004). For species in which only males are harvested, the standard model that does not take breeding system into account allows for 1.8% and 2.3% of the carnivore or herbivore population respectively to be shot before lambda falls below 1. The tailored models, however, allowed more animals to be removed: 5.1% of lions to be shot, 6.8% of impala, and 6.0% of kudu, surprisingly high figures. Only for steinbok does knowledge of breeding system lower sustainable harvest with 1.0% being removed before the population starts to decline. Thus, depending on the species, breeding system assumptions raise or lower sustainable offtake by a considerable amount when male offtake is the mode of removal. The large increase in sustainable offtake is due to the effect of harem size because large harems (h = 5 10) allow greater numbers of males to be harvested. The 56%